Impact of the COVID-19 pandemic on the detection of

http://dx.doi.org/10.5588/ijtld.20.0539

                                                                            LETTER

Impact of the COVID-19 pandemic on the detection of
TB in Shanghai, China

Z. Wu,1,2 J. Chen,2 Z. Xia,2 Q. Pan,2 Z. Yuan,2 W. Zhang,1 X. Shen2

1
    Department of Infectious Diseases, Huashan Hospital, Fudan University, Shanghai,
2
    Department of Tuberculosis Control, Shanghai Municipal Center for Disease Control
and Prevention, Shanghai, China

Correspondence to: Xin Shen, Department of Tuberculosis Control, Shanghai
Municipal Center for Disease Control and Prevention, 1380 Zhongshanxi Road,
Changing District, Shanghai, China. e-mail: shenxin@scdc.sh.cn

Dear Editor,
TB remains a major public health threat globally, but the TB epidemic may be
exacerbated by the COVID-19 pandemic.1,2 Reports have suggested that TB detection
and health care has declined during lockdown.3,4 To contain the spread of COVID-19,
Shanghai, China (population: 24 million) initiated a Level 1 public health emergency
response5 on 24 January 2020 (at the beginning of the Chinese New Year holiday
[CNY]). Public gatherings were banned, travel restrictions imposed and social
distancing implemented.6 Medical resources (both health care workers and materials)
were prioritised for COVID-19. Six of 26 county-level TB clinics were closed and
two of four tertiary TB hospitals halved outpatient visits and the number of hospital
beds. On 24 March, the emergency response was lowered to Level 2. With social
distancing still in effect, people began to resume work and return to normal life, and
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hospitals gradually returned to routine work. This study aims to examine the impact of
the COVID-19 on TB detection in Shanghai during this period.
    This was a cross-sectional study using routinely collected TB control programme
data and public COVID-19 data. TB patients were diagnosed and reported as per the
Chinese national standard of diagnosis for TB.7 We included all bacteriologically
confirmed and clinically diagnosed TB patients identified from 1 November 2019
through to 28 May 2020. Patients identified in the same period of 2018–2019 (from 1
November 2018 through 29 May 2019) were also enrolled for comparison. The
number of days were identical because of the leap year in 2020. We calculated and
plotted weekly notification rates (notified cases per 1,000,000 person-weeks) of TB
and local COVID-19, with lines smoothed using the Loess method.
    We divided the study period into three parts: pre-lockdown (from 1 November
2019 to 23 January 2020), lockdown (from 24 January to 26 March 2020) and
post-lockdown (from 27 March to 28 May 2020). We used 26 March instead of 23
March as the end of the lockdown period to avoid the split in a whole week.
Notification rates during the lockdown and post-lockdown periods were compared
with those in the pre-lockdown period. These rates were also compared with those
during their corresponding periods in 2018–2019. Incidence rate ratios (IRRs) and
95% confidence intervals (CIs) (calculated using exact methods [mid-p]) were used
for the comparisons between periods. Demographic and clinical characteristics were
compared between patients reported in the pre-lockdown and lockdown periods in
2019–2020. Diagnosis delay was defined as days from the date of self-reported onset
of TB-related symptoms to the date when TB was confirmed or clinically diagnosed.
The analysis was performed using R® Software v3.6.2 (R Computing, Vienna,
Austria). P < 0.05 was considered significant.
    The study was approved by the Ethical Review Committee at Shanghai Municipal
Center for Disease Control and Prevention, Shanghai, China. Since only anonymised
secondary data were used, no informed consent was sought.
    The data for 727,199,820 person-weeks and 2846 TB cases from 1 November

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2019 to 28 May 2020 were analysed. The TB notification rate decreased by 47.8%
from 4.6 (95%CI 4.3–4.8) per 1,000,000 person-weeks during the pre-lockdown
period to 2.4 (95%CI 2.2–2.6) per 1,000,000 person-weeks during the lockdown
period (IRR 0.5, 95% CI 0.5–0.6; P < 0.001). Case notifications began to rebound in
mid- to late-February 2020 (because COVID-19 rates declined), and kept rising
steadily after the lockdown order was lifted (see Figure). The rate in the
post-lockdown period was almost the same as that in the pre-lockdown period
(post-lockdown: 4.5 vs. pre-lockdown: 4.6, per 1,000,000 person-weeks; IRR 1.0,
95% CI 0.9–1.1; P = 0.774). When compared with those in the same periods in
2018–2019, the rates during the lockdown (IRR 0.6, 95% CI 0.5–0.7; P < 0.001) and
post-lockdown (IRR 0.9, 95% CI 0.8–1.0; P = 0.009) periods were significantly lower,
while the rate during the pre-lockdown period remains similar (IRR 1.0, 95% CI
0.9–1.0; P = 0.179).
    Demographic and clinical characteristics such as age, sex, residents or migrants,
new or previously treated patients, and with or without cavity on X-ray varied little
between patients reported in the pre-lockdown and lockdown periods (all P > 0.05).
However, patients identified during the lockdown period had less access to sputum
smear examination (pre-lockdown: 95.7% vs. lockdown: 86.2%, P < 0.001) and
Xpert® MTB/RIF testing (Cepheid, Sunnyvale, CA, USA) (pre-lockdown: 79.5% vs.
lockdown: 66.9%; P < 0.001), but more diagnosis delays (pre-lockdown: 15,
interquartile range [IQR] 6–29 vs. lockdown: 18.5, IQR 9–33; P < 0.001).
    We observed a significant decline in TB detection during the COVID-19
pandemic in Shanghai, more than that reported in Korea, Japan, and Taiwan.8–10 This
might be caused by more aggressive public health strategies adopted in Shanghai6
owing to its close link to the epicentre in Wuhan, Hubei Province. One study found
TB diagnoses dropped during holidays due to reduced clinical activities,11 which may
well explain the decline in TB notification rates during the CNY holiday in 2019, as
rates increased as the holiday ended. However, the drop in 2020 was more
pronounced and the upturn occurred at least 2 weeks after the end of the CNY holiday,

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which indicated the effect of the COVID-19 pandemic. During the pandemic, people
reduced seeking health care due to insufficient and delayed provision of TB
services.4,12,13 We also observed that the lockdown period led to poor access to
diagnostic tests and prolonged diagnosis delay for TB patients. Lai et al.10 suggested
that social distancing helped to reduce TB incidence via control of TB transmission.
In Shanghai, the TB notification rates increased rapidly after the lockdown order was
lifted and approached the level of the same period in 2019. Because TB has a long
incubation period, the benefit of short-term transmission control measures on TB
incidence is reduced.9,14 As the Figure indicates, the upturn in the TB notification rates
occurred in mid- to late February 2020, when the COVID-19 rates began to decline.
This might be explained by the resulting transfer of medical resources from
combating COVID-19 (as its incidence declined) back to TB services. This also
emphasises the need to build an emergency response programme to ensure ongoing
TB health care during any future pandemic.
    A limitation of this study is the potential underestimate of TB detection during the
pandemic due to the use of notification data. Although TB is compulsorily notifiable,
it might be underreported because of insufficient TB care staff during the pandemic.
    In conclusion, the detection of TB was adversely impacted by COVID-19 in
Shanghai, China. It is necessary to improve emergency response programmes to
minimise the effects of COVID-19 (and any future emerging pathogen) on the control
of TB and other chronic infectious diseases.

Acknowledgements
This work was supported by the Chinese National Science and Technology Major
Project (2018ZX10715012) and National Natural Science Foundation of China,
Beijing, China (81872679). The sponsors of the study had no role in study design,
data collection, data analysis, data interpretation, or writing of the manuscript.
    Conflicts of interest: none declared.

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Figure. Weekly notification rates for TB from 1 November to 28 May during both
2018–2019 and 2019–2020 in Shanghai, China, against the notification rates of the
COVID-19. The solid line and solid circles indicate TB notification rates in
2018–2019, whereas the dashed line and hollow circles indicate those in 2019–2020.
Extrapulmonary TB and tuberculous pleurisy cases were excluded. The dotted line
and hollow triangles show the rate of COVID-19. Only local COVID-19 cases were
included (imported cases were excluded). Notification rates are given as cases per
1,000,000 person-weeks.

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